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Korean Society of Life Science (한국생명과학회)
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Sexual Reproduction in Unicellular Green Alga Chlamydomonas

수염녹두말속(Chlamydomonas) 단세포 녹조의 유성생식

  • Lee, Kyu Bae (Department of Biological Science Education, Chosun University)
  • Received : 2017.01.03
  • Accepted : 2017.01.23
  • Published : 2017.01.30
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Abstract

The sexual reproduction of the unicellular green alga Chlamydomonas is reviewed for a comprehensive understanding of the complex processes. The sexual life cycle of C. reinhardtii is distinguished into five main stages: gametogenesis, gamete activation, cell fusion, zygote maturation, and meiosis and germination. Gametogenesis is induced by nitrogen starvation in the environment. C. reinhardtii has two mating types: mating type plus ($mt^+$) and mating type minus ($mt^-$), controlled by a single complex mating type locus ($MT^+$ or $MT^-$) on linkage group VI. In the early gametogenesis agglutinins are synthesized. The $mt^+$ and $mt^-$ agglutinins are encoded by the autosomal genes SAG1 (Sexual AGglutination1) and SAD1 (Sexual ADhesion1), respectively. The agglutinins are responsible for the flagellar adhesion of the two mating type of gametes. The flagellar adhesion initiates a cAMP mediated signal transduction pathways and activates the flagellar tips. In response to the cAMP signal, mating structures between two flagella are activated. The $mt^+$ and $mt^-$ gamete-specific fusion proteins, Fus1 and Hap2/Gcs1, are present on the plasma membrane of the two mating structures. Contact of the two mating structures leads to develop a fertilization tubule forming a cytoplasmic bridge between the two gametes. Upon fusion of nuclei and chloroplasts of $mt^+$ and $mt^-$ cells, the zygotes become zygospores. It is notable that the young zygote shows uniparental inheritance of chloroplast DNA from the $mt^+$ parent and mitochondrial DNA from the $mt^-$ parent. Under the favorable conditions, the zygospores divide meiotically and germinate and then new haploid progenies, vegetative cells, are released.

이 논문은 다세포 녹색식물의 조상으로 생각되는 단세포인 수염녹두말속(Chlamydomonas) 녹조의 복잡한 유성생식 과정을 종합적으로 이해하기 위해서 기술되었다. 모델생물로 알려진 클래미도모나스 레인하르티(Chlamydomonas reinhardtii)의 유성생식 생활사는 배우자발생, 배우자 활성화, 세포융합, 접합자 성숙, 감수분열과 발아 등의 다섯 시기로 구별된다. 배우자발생은 서식지에서 질소가 결핍되어 시작된다. 그 결과, 교배형 유전자자리($MT^+$ 또는 $MT^-$)에 의해 조절된 두 가지 교배형($mt^+$ 및 $mt^-$)의 배우자들이 발생된다. 유성생식을 위한 두 번째 자극원인 청색광이 교배능력을 갖고 있지 않는 예비배우자 세포에 조사되면 교배능력을 가진 배우자로 분화된다. 배우자발생의 초기에, 두 배우자 세포들은 응집소(agglutin) 분자들을 합성한다. 즉, $mt^+$ 응집소 및 $mt^-$ 응집소는 상염색체에 있는 성응집(SAG1) 및 성접착(SAD1) 유전자들이 발현되어 각각 합성된다. 응집소들에 의해서 두 배우자 세포들의 편모가 접착되면 cAMP가 신호전달 경로를 작동시켜서 편모의 끝 부부을 활성화시킨다. cAMP의 신호에 반응하여 두 배우자들의 세포벽이 벗겨지고 2개의 편모 사이에서 각각의 교배구조(mating structure)가 발달한다. 교배구조의 원형질막에는 $mt^+$ 및 $mt^-$ 배우자-특이 융합 단백질인 Fus1 및 Hap2/Gcs1이 있다. 이 단백질들의 상호작용으로 두 교배구조가 접촉되면, 두 배우자 사이에 세포질이 연결되어 수정세관(fertilization tubule)이 발달한다. $mt^+$ 및 $mt^-$ 배우자들의 핵과 엽록체가 융합되면 2배체의 접합자가 형성된다. 그 후 배우자들의 특성은 사라지며 융합단백질들(Fus1 및 Hap2)이 분해되고 접합자-특이(zygote-specific) 유전자들이 활성화 된다. 접합자는 24시간에 걸쳐 두꺼운 세포벽을 가진 접합포자(zygospore)로 발달한다. 어린 접합자에서 교배 후 60분 이내에 $mt^-$ 엽록체 DNA와 $mt^+$ 미토콘드리아 DNA가 선택적으로 제거된다. 따라서 이 두 소기관들은 각각 $mt^-$ 미토콘드리아 DNA와 $mt^+$ 엽록체 DNA만 남아서 단친유전(uniparental inheritance)이 이루어진다. 적당한 조건이 되면 접합포자가 감수분열과 발아 과정을 거쳐 반수체 영양세포가 방출되어 새로운 세대가 다시 시작된다.

Keywords

References

  1. Abedin, M. and King, N. 2010. Diverse evolutionary paths to cell adhesion. Trends Cell Biol. 20, 734-742. https://doi.org/10.1016/j.tcb.2010.08.002
  2. Adair, W. S., Hwang, C. J. and Goodenough, U. W. 1983. Identification and visualization of the sexual agglutinin from the mating-type plus flagellar membrane of Chlamydomonas. Cell 33, 83-193.
  3. Adair, W. S., Monk, B. C., Cohen, R., Hwang, C. and Goodenough, U. W. 1982. Sexual agglutinins from the Chlamydomonas flagellar membrane: Partial purification and characterization. J. Biol. Chem. 257, 4593-4602.
  4. Adair,W. S., Steinmetz, S. A., Mattson, D. M., Goodenough, U. W. and Heuser, J. E. 1987. Nucleated assembly of Chlamydomonas and Volvox cell walls. J. Cell Biol. 105, 2373-2382. https://doi.org/10.1083/jcb.105.5.2373
  5. Adams, M. W., Huang, B. and Luck, D. J. L. 1982. Temperature-sensitive, assembly-defective flagella mutants of Chlamydomonas reinhardtli. Genetics 100, 579-586.
  6. Aoyama, H., Hagiwara, Y., Misumi, O. and Kuroiwa, T. 2006. Complete elimination of maternal mitochondrial DNA during meiosis resulting in the paternal inheritance of the mitochondrial genome in Chlamydomonas species. Protoplasma 28, 231-242.
  7. Aoyama, H., Saitoh, S., Kuroiwa, T. and Nakamura, S. 2014. Comparative analysis of zygospore transcripts during early germination in Chlamydomonas reinhardtii. J. Plant Physiol. 171, 1685-1692. https://doi.org/10.1016/j.jplph.2014.07.016
  8. Arakaki, Y., Kawai-Toyooka, H., Hamamura, Y., Higashiyama, T., Noga, A., Hirono, M., Olson, B. J. S. C. and Nozaki, H. 2013. The Simplest integrated multicellular organism unveiled. PLoS ONE 8, e81641. doi:10.1371/journal.pone.0081641.
  9. Armbrust, E. V., Ferris, P. J. and Goodenough, U. W. 1993. A mating type-linked gene cluster expressed in Chlamydomonas zygotes participates in the uniparental inheritance of the chloroplast genome. Cell 74, 801-811. https://doi.org/10.1016/0092-8674(93)90460-8
  10. Beck, C. F. and Acker, A. 1992. Gametic Differentiation of Chiamydomonas reinhardtii: Control by nitrogen and light. Plant Physiol. 98, 822-826. https://doi.org/10.1104/pp.98.3.822
  11. Beck, C. F. and Haring, M. A. 1996. Gametic differentiation of Chlamydomonas. Int. Rev. Cytol. 168, 259-302.
  12. Birky, C. W. Jr. 2001 The inheritance of genes in mitochondria and chloroplasts: Laws, mechanisms, and models. Proc. Natl. Acad. Sci. USA 35, 125-148.
  13. Birky, C. W. Jr. 2008. Uniparental inheritance of organelle genes. Cur. Biol. 18, 692-295. https://doi.org/10.1016/j.cub.2008.06.049
  14. Blaby, I. K., Blaby-Haas, C. E., Tourasse, N., Hom, E. F. Y., Lopez, D., Aksoy, M,, Grossman, A., Umen, J., Dutcher, S., Porter, M., King, S., Witman, G. B., Stanke, M., Harris, E. H., Goodstein, D., Grimwood, J., Schmutz, J., Vallon,.O., Merchant, S. S. and Prochnik, S. 2014. The Chlamydomonas genome project: a decade on. Trends in Plant Sci. 19, 672-680.
  15. Blank, R., Grobe, B. and Arnold, C. G. 1978. Time-sequence of nuclear and chloroplast fusions in the zygote of Chlamydomonas reinhardtii. Planta 138, 63-64. https://doi.org/10.1007/BF00392916
  16. Boyd, J. S., Mittelmeier, T. M. and Dieckmann, C. L. 2011. New insights into eyespot placement and assembly in Chlamydomonas. BioArchitecture 1, 196-199. https://doi.org/10.4161/bioa.1.4.17697
  17. Boynton, J. E., Harris, E. H., Burkhart, B. D., Lamerson, P. M. and Gillham, N. W. 1987. Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc. Natl. Acad. Sci. USA 84, 2391-2395. https://doi.org/10.1073/pnas.84.8.2391
  18. Breton, G. and Kay, S. 2006 Circadian rhythms lit up in Chlamydomonas. Genome Biol. 7, art no. 215.
  19. Brown, R. M., Johnsin, S. C. and Bold, H. C. 1968. Electron and phase-contrast microscopy of sexual reproduction in Chlamydomonas moewusii. J. Phycology 4, 100-120. https://doi.org/10.1111/j.1529-8817.1968.tb04683.x
  20. Cooper, J. B., Adair, W. S., Mecham, R. P., Heuser, J. E. and Goodenough, U. W. 1983. Chlamydomonas agglutinin is a hydroxyproline-rich glycoprotein. Proc. Natl. Acad. Sci. USA 80, 5898-5901. https://doi.org/10.1073/pnas.80.19.5898
  21. Cross, F. R. and Umen, J. G. 2015 The Chlamydomonas cell cycle. The Plant J. 82, 370-392. https://doi.org/10.1111/tpj.12795
  22. Demets, R., Tomson, A. M., Haman, W. L., Stegwee, D. and van den Ende, H. 1988. Cell-cell adhesion in conjugating Chlamydomonas gametes: a self-enhancing process. Protoplasma 145, 27-36. https://doi.org/10.1007/BF01323253
  23. Detmers, P. A., Carboni, J. M. and Condeelis, J. 1985. Localization of actin in Chlamydomonas using anti-actin and NBDphallacidin. Cell Motil. 5, 415-430. https://doi.org/10.1002/cm.970050505
  24. Detmers, P. A., Goodenough, U. W. and Condeelis, J. 1983. Elongation of the fertilization tubule in Chlamydomonas: New observations on the core microfilaments and the effect of transient intracellular signals on their structural integrity. J. Cell Biol. 97, 522-532. https://doi.org/10.1083/jcb.97.2.522
  25. Ehler, L. L. and Dutcher, S. K. 1998. Pharmacological and genetic evidence for a role of rootlet and phycoplast microtubules in the positioning and assembly of cleavage furrows in Chlamydomonas reinhardtii. Cell Motil. Cytoskeleton 40, 193-207. https://doi.org/10.1002/(SICI)1097-0169(1998)40:2<193::AID-CM8>3.0.CO;2-G
  26. Ehler, L. L., Holmes, J. A. and Dutcher, S. K. 1995. Loss of spatial control of the mitotic spindle apparatus in a Chlamydomonas reinhardtii mutant strain lacking basal bodies. Genetics 141, 945-960.
  27. Ferris, P. J., Armbrust, E. V. and Goodenough, U. W. 2002. Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160, 181-200.
  28. Ferris, P. J. and Goodenough, U. W. 1985. Transcription of novel genes, including a gene linked to mating-type locus, induced by Chlamydomonas fertilization. Mol. Cell Biol. 7, 2360-2366.
  29. Ferris, P. J. and Goodenough, U. W. 1994. The mating-type locus of Chlamydomonas reinhardtii contains highly rearranged DNA sequences. Cell 76, 1135-1145. https://doi.org/10.1016/0092-8674(94)90389-1
  30. Ferris, P. J. and Goodenough, U. W. 1997. Mating type in Chlamydomonas is specified by mid, the minus dominance gene. Genetics 146, 859-869.
  31. Ferris, P. J., Waffenschmidt, S., Umen, J. G., Lin, H., Lee, J-H., Ishida, K., Kubo, K., Lau, J., and Goodenough, U. W. 2005. Plus and minus sexual agglutinins from Chlamydomonas reinhardtii. Plant Cell 17, 597-615. https://doi.org/10.1105/tpc.104.028035
  32. Ferris, P. J., Woessner, J.P. and Goodenough, U. W. 1996. A sex recognition glycoprotein is encoded by the plus mating- type gene fus1 of Chlamydomonas reinhardtii. Mol. Biol. Cell 7, 1235-1248. https://doi.org/10.1091/mbc.7.8.1235
  33. Friedmann, I., Colwin, A. L. and Colwin, L..H. 1968. Finestructural aspects of fertilization in Chlamydomonas reinhardtii. J. Cell Sci. 3, 115-128.
  34. Galloway, R. E. and Goodenough, U. W. 1985. Genetic analysis of mating locus linked mutations in Chlamydomonas reinhardtii. Genetics 111, 447-461.
  35. Gillham, N. W. 1978. Organelle heredity. Raven Press, New York, NY. USA.
  36. Goodenough, U. W. 1989. Cyclic AMP enhances the sexual agglutinability of Chlamydomonas flagella. J. Cell Biol. 109, 247-252. https://doi.org/10.1083/jcb.109.1.247
  37. Goodenough, U. R. and Jurivich, D. 1978. Tipping and mating-structure activation induced in Chlamydomonas gamates by flagellar membrane antisera. J. Cell Biol. 79, 680-693. https://doi.org/10.1083/jcb.79.3.680
  38. Goodwnough, U. W. and Weiss, R. L. 1975. Gametic differentiation Chlamydomonas reinhardtii. III. Cell wall lysis and microfilament-associated ,ating structure activation in wildtype and mutant strains J. Cell Biol. 67, 623-637. https://doi.org/10.1083/jcb.67.3.623
  39. Goodenough, U. W., Detmers, P. A. and Hwang, C. 1982. Activation for cell fusion Chlamydomonas: Analysis of wildtype gametes and nonfusing mutants. J. Cell Biol. 92, 378-386. https://doi.org/10.1083/jcb.92.2.378
  40. Goodenough, U. W., Lin, H. and Lee, J. H. 2007. Sex determination in Chlamydomonas. Semin. Cell Dev. Biol. 18, 350-361. https://doi.org/10.1016/j.semcdb.2007.02.006
  41. Goodenough, U. W., Adair, W. S., Collin-Osdoby, P. and Heuser, J. E. 1985. Structure of the Chlamydomonas agglutinin and related flagellar surface proteins in vitro and in situ. J. Cell Biol. 101, 924-941. https://doi.org/10.1083/jcb.101.3.924
  42. Goodenough, U. W., Armbrust, E. V., Campbell, A. M. and Ferris, P. J. 1995. Molecular genetics of sexuality in Chlamydomonas. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 21-44. https://doi.org/10.1146/annurev.pp.46.060195.000321
  43. Grant, D. and Chiang, K. S. 1980. Physical mapping and characterization of Chlamydomonas mitochondrial DNA molecules: their unique ends, sequence homogeneity, and conservation. Plasmid 4, 82-96. https://doi.org/10.1016/0147-619X(80)90085-2
  44. Grosberg, R. K. and Strathmann, R. R. 2007. The evolution of multicellularity: A minor major transition?. Annu. Rev. Ecol. Evol. Syst. 38, 621-654. https://doi.org/10.1146/annurev.ecolsys.36.102403.114735
  45. Grossman, A. R., Harris, E. E., Hauser, C., Lefebvre, P. A., Martinez, D., Rokhsar, D., Shrager, J., Silflow, C. D., Stern. D.,Vallon, O. and Zhang, Z. D. 2003. Chlamydomonas reinhardtii at the crossroads of genomics. Eukaryot. Cell 2, 1137-1150. https://doi.org/10.1128/EC.2.6.1137-1150.2003
  46. Guiry, M. D. and Guiry, G. M. 2016 AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org/. Accessed on 06 April 2016.
  47. Hallmann, A. 2003. Extracellular matrix and sex-inducing pheromone in Volvox. Int. Rev. Cytol. 227, 131-182.
  48. Hallmann, A. 2011. Evolution of reproductive development in the volvocine algae. Sex Plant Reprod 24, 97-112. https://doi.org/10.1007/s00497-010-0158-4
  49. Harris, E. H. 1989. The Chlamydomonas Sourcebook: A comprehensive guide to biology and laboratory Use. Academic Press, San Diego, USA.
  50. Harris, E. H. 2001. Chlamydomonas as a model organism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 363-406. https://doi.org/10.1146/annurev.arplant.52.1.363
  51. Harris, E. H. 2009a. The Chlamydomonas Sourcebook, 2nd ed. Academic Press, NY, USA.
  52. Harris, E. H. 2009b. The Chlamydomonas Sourcebook: Introduction to Chlamydomonas and its laboratory use, 2nd ed. Academic Press, Oxford, USA.
  53. Harris, E. H., Stern, D. B. and Witman, G. B. 2009. The Chlamydomonas sourcebook, 2nd ed. Academic Press, San Diego. USA.
  54. Hegemann, P. 2008. Algal sensory photoreceptors. Annu. Rev. Plant Biol. 59, 167-187. https://doi.org/10.1146/annurev.arplant.59.032607.092847
  55. Herron, M. D. and Michod, R. E. 2008. Evolution of complexity in the volvocine algae: Transitions in individuality through Darwin's eye. Evolution 62, 436-451. https://doi.org/10.1111/j.1558-5646.2007.00304.x
  56. Herron, M. D. and Nedelcu, A. M. 2015. Volvocine Algae: From simple to complex multicellularity, pp 120-152. In: Ruiz-Trillo, I. and Nedelcu, A. M. (eds.,), Evolutionary Transitions to Multicellular Life, Advances in Marine Genomics 2, doi 10.1007/978-94-017-9642-2_7.
  57. Herron, M. D., Hackett, J. D., Aylward, F. O. and Michod, R. E. 2009. Triassic origin and early radiation of multicellular volvocine algae. Proc. Nati. Acad. Sci. USA 106, 3254-3258. https://doi.org/10.1073/pnas.0811205106
  58. Hoffmann, X. K. and Beck, C. F. 2005. Mating-induced shedding of cell walls, removal of walls from vegetative cells, and osmotic stress induce presumed cell wall genes in Chlamydomonas. Plant Physiol. 139, 999-1014. https://doi.org/10.1104/pp.105.065037
  59. Holmes, J. A. and Dutcher, S. K. 1989. Cellular asymmetry in Chlamydomonas reinhardtii. J. Cell Sci. 94, 273-285.
  60. Huang, K. and Beck, C. F. 2003. Phototropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii. Proc. Nat. Acad. Sci. USA 100, 6269-6274. https://doi.org/10.1073/pnas.0931459100
  61. Huang, K., Kunkel, T. and Beck, C. F. 2004. Localization of the blue-light receptor phototropin to the flagella of the green alga Chlamydomonas reinhardtii. MBoC 15, 3605-3614. https://doi.org/10.1091/mbc.e04-01-0010
  62. Huang, K., Merkle, T. and Beck, C. F. 2002. Isolation and characterization of a Chlamydomonas gene that encodes a putative blue-light photoreceptor of the phototropin family. Physiol. Plant 115, 613-622. https://doi.org/10.1034/j.1399-3054.2002.1150416.x
  63. Huang, B., Rifkin, M. R. and Luck, D. J. L. 1977 Temperature-sensitive mutations affecting flagellar assembly and function in Chlamydomonas reinhardtii. J. Cell Biol. 72, 67-85. https://doi.org/10.1083/jcb.72.1.67
  64. Hunnicutt, G. R., Kosfiszer, M. G. and Snell, W. J. 1990. Cell body and flagellar agglutinins in Chlamydomonas reinhardtii: The cell body plasma membrane is a reservoir for agglutinins whose migration to the flagella is regulated by a functional barrier. J. Cell Biol. 111, 1605-1616. https://doi.org/10.1083/jcb.111.4.1605
  65. Iomini, C., Babaev-Khaimov, V., Sassaroli, M. and Piperno, G. 2001. Protein particles in Chlamydomonas flagella undergo a transport cycle consisting of four phases. J. Cell Biol. 153, 13-24. https://doi.org/10.1083/jcb.153.1.13
  66. Johnson, M. A. 2010. Fertilization: Monogamy by mutually assured destruction. Cur. Biol. 20, 571-573. https://doi.org/10.1016/j.cub.2010.05.026
  67. Johnson, M. A., von Besser, K., Zhou, Q., Smith, E., Aux, G., Patton, D., Levin, J. Z. and Preuss, D. 2004. Arabidopsis hapless mutations define essential gametophytic functions. Genetics 168, 971-982. https://doi.org/10.1534/genetics.104.029447
  68. Kinoshita, T., Fukuzawa, H., Shimada, T., Saito, T. and Matsuda, Y. 1992. Primary structure and expression of a gamete lytic enzyme in Chlamydomonas reinhardtii: similarity of functional domains to matrix metalloproteases. Proc. Natl. Acad. Sci. USA. 89, 4693- 4697. https://doi.org/10.1073/pnas.89.10.4693
  69. Kates, J. R. and Jones, R. F. 1964. Variation in dehygrogenase and glutamate dehydrogenase during the synchronous development of Chlamydomonas. Biochim. Biophys. Acta. 86, 438-447. https://doi.org/10.1016/0304-4165(64)90083-2
  70. Kirk, D. L. 1998a. Volvox. Cambridge University Press, Cambridge, UK.
  71. Kirk, D. L. 1998b. Volvox: molecular-genetic origins of multicellularity and cellular differentiation. Developmental and cell biology series. Cambridge University Press, Cambridge, UK.
  72. Knoll, A. H. 2011. The multiple origins of complex multicellularity. Annu. Rev. Earth Planet Sci. 39, 217-239. https://doi.org/10.1146/annurev.earth.031208.100209
  73. Kozminski, K. G., Johnson, K. A., Forscher, P. and Rosenbaum, J. L. 1993. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc. Natl. Acad. Sci. USA 90, 5519-5523. https://doi.org/10.1073/pnas.90.12.5519
  74. Kubo, T., Abe, J., Oyamada, T., Ohnishi, M., Fukuzawa, H., Matsuda, Y. and Saito, T. 2008. Characterization of novel genes induced by sexual adhesion and gamete fusion and of their transcriptional regulation in Chlamydomonas reinhardtii. Plant Cell Physiol. 49, 981-993. https://doi.org/10.1093/pcp/pcn076
  75. Kuroiwa, T. 1991. The replication, differentiation and inheritance of plastids with emphasis on the concept of organelle nuclei. Int. Rev. Cytol. 128, 1-62.
  76. Kuroiwa, T. 2010a. Review-mechanisms of organelle division and inheritance and their implications regarding the origin of eukaryotic cells. Proc. Jpn. Acad. Ser. 86, 455-470. https://doi.org/10.2183/pjab.86.455
  77. Kuroiwa, T. 2010b. Review of cytological studies on cellular and molecular mechanisms of uniparental (maternal or paternal) inheritance of plastid and mitochondrial genomes induced by active digestion of organelle nuclei (nucleoids). J. Plant Res. 123, 207-230. https://doi.org/10.1007/s10265-009-0306-9
  78. Kuroiwa, T., Suzuki, T., Ogawa, K. and Kawano, S. 1981. The chloroplast nucleus: Distribution, number, size, and shape, and a model for the multiplication of the chloroplast genome during chloroplast development. Plant Cell Physiol. 22, 381-396.
  79. Kuroiwa, T., Kawano, S., Nishibayashi, S. and Sato, C. 1982. Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298, 481-483. https://doi.org/10.1038/298481a0
  80. Kurvari, V., Grishin, N. V. and Snell, W. J. 1998 A gametespecific, sex-limited homeodomain protein in Chlamydomonas. J. Cell Biol. 143, 1971-1980. https://doi.org/10.1083/jcb.143.7.1971
  81. Lee, J. H., Lin, H., Joo, S. and Goodenough, U. W. 2008. Early sexual origins of homeoprotein heterodimerization and evolution of the plant KNOX/BELL family. Cell 133, 829-840. https://doi.org/10.1016/j.cell.2008.04.028
  82. Lee, J. H., Waffenschmidt, S., Small, L. and Goodenough, U. W. 2007. Between-species analysis of short-repeat modules in cell wall and sex-related hydroxyproline-rich glycoproteins of Chlamydomonas. Plant Physiol. 144, 1813-1826. https://doi.org/10.1104/pp.107.100891
  83. Lechtreck, K. F., Rostmann, J. and Grunow, A. 2002. Analysis of Chlamydomonas SF-assemblin by GFP tagging and expression of antisense constructs. J. Cell Sci. 115, 1511-1522.
  84. Lechtreck, K. F. and Silflow, C. D. 1997. SF-assemblin in Chlamydomonas: sequence conservation and localization during the cell cycle. Cell Motil. Cytoskeleton 36, 190-201. https://doi.org/10.1002/(SICI)1097-0169(1997)36:2<190::AID-CM8>3.0.CO;2-D
  85. Lin, H. and Goodenough, U. W. 2007. Gametogenesis in the Chlamydomonas reinhardtii minus mating type is controlled by two genes, MID and MTD1. Genetics 176, 913-925.
  86. Liu, Y., Misamore, M. J. and Snell, W. J. 2010. Membrane fusion triggers rapid degradation of two gamete-specific, fusion-essential proteins in a membrane block to polygamy in Chlamydomonas. Development 137, 1473-1481. https://doi.org/10.1242/dev.044743
  87. Liu, Y., Tewari, R., Ning, J., Blagborough, A. M., Garbom, S., Pei, J., Grishin, N. V., Steele, R. E., Sinden, R. E., Snell, W. J. and Billker, O. 2008. The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes. Genes Dev. 22, 1051-1068. https://doi.org/10.1101/gad.1656508
  88. Malmberg, A. E. and VanWinkle-Swift, K. P. 2001. Zygospore germination in Chlamydomonas monoica (Chlorophyceae): timing and pattern of secondary zygospore wall degradation in relation to cytoplasmic events. J. Phycol. 37, 86-94. https://doi.org/10.1046/j.1529-8817.2001.037001086.x
  89. Matsuda, Y., Shimada, T. and Sakamoto, Y. 1992. Ammonium ions control gametic differentiation in Chlamydomonas reinhardtii. Plant Cell Physiol. 33, 909-914.
  90. Matsuo, T. and Ishiura, M. 2011. Chlamydomonas reinhardtii as a new model system for studying the molecular basis of the circadian clock. FEBS Lett. 585, 1495-1502. https://doi.org/10.1016/j.febslet.2011.02.025
  91. Mesland, D. A. M. 1976. Mating in Chlamvdomonas eugamaros, a scanning electron microscopical study. Arch. Microbial. 109, 31-35. https://doi.org/10.1007/BF00425109
  92. Mesland, D. A. M., Hoffman, J. L., Califor, E. and Goodenough, U. W. 1980. Flagellar tip activation stimulated by membrane adhesions in Chlamydomonas gametes. J. Cell Biol. 84, 599-617. https://doi.org/10.1083/jcb.84.3.599
  93. McFadden, D. E., Kwong, L. C., Yam, I. Y. and Langlois, S. 1993. Parental origin of triploidy in human fetuses: evidence for genomic imprinting. Hum. Genet. 92, 465-469. https://doi.org/10.1007/BF00216452
  94. Merchant, S. S., Prochnik, S. E., Vallon, O., Harris, E. H. and Karpowicz, S. J. et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-251. https://doi.org/10.1126/science.1143609
  95. Michod, R. E. 2005. On the transfer of fitness from the cell to the multicellular organism. Biol. Philos. 20, 967-987.
  96. Minami, S. and Goodenough, U. W. 1978. Novel glycopolypeptide synthesis induced by gametic cell fusion in Chlamydomonas reinhardtii. J. Cell Biol. 77, 165-181. https://doi.org/10.1083/jcb.77.1.165
  97. Misamore, M. J., Gupta, S. and Snell, W. J. 2003. The Chlamydomonas Fus1 protein is present on the mating type plus fusion organelle and required for a critical membrane adhesion event during fusion with minus gametes. Mol. Biol. Cell 14, 2530-2542. https://doi.org/10.1091/mbc.e02-12-0790
  98. Mittelmeier, T. M., Boyd, J. S., Lamb, M. R. and Dieckmann, C. L. 2011. Asymmetric properties of the Chlamydomonas reinhardtii cytoskeleton direct rhodopsin photoreceptor localization J. Cell Biol. 193, 741-753. https://doi.org/10.1083/jcb.201009131
  99. Mittelmeier, T. M., Thompson, M. D., ozturk, E. and Dieckmanna, C. L. 2013. Independent localization of plasma membrane and chloroplast components during eyespot assembly. Eukaryot. Cell 12, 1258-1270. https://doi.org/10.1128/EC.00111-13
  100. Miyamura, S., Mogi, Y., Mitsuhashi, F., Kawano, S. and Nagumo, T. 2009. Visualizing the spatial arrangement of flagella-eyespots-cell fusion sites in gametes and planozygotes of Chlamydomonas reinhardtii (Chlorophyceae, Chlorophyta) with high-resolution FE-SEM. Cytologia 74, 409-415. https://doi.org/10.1508/cytologia.74.409
  101. Mori, T., Kuroiwa, H., Higashiyama, T. and Kuroiwa, T. 2006. GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat. Cell Biol. 8, 64-71. https://doi.org/10.1038/ncb1345
  102. Morris, R. L., Keller, L. R., Zweidler, A. and Rizzo, P. J. 1990. Analysis of Chlamydomonas reinhardtii histones and chromatin. J. Protozool. 37, 117-123. https://doi.org/10.1111/j.1550-7408.1990.tb05880.x
  103. Nakada, T., Misawa, K. and Nozaki, H. 2008. .Molecular systematic of Volvocales (Chlorophyceae, Chlorophyta) based on exhaustive 18S rRNA phylogenetic analyses. Mol. Phylogenet. Evol. 48, 281-291. https://doi.org/10.1016/j.ympev.2008.03.016
  104. Navara, C. S., First, N. L. and Schatten, G. 1994. Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: the role of the sperm aster. Dev. Biol. 162, 29-40. https://doi.org/10.1006/dbio.1994.1064
  105. Niklas, K. J. 2014. The evolutionary-developmental origin of multicellularlity. Am. J. Bot. 101, 6-25. https://doi.org/10.3732/ajb.1300314
  106. Ning. J., Otto, T. D., Pfander, C., Schwach, F., Brochet, M., Bushell, E., Goulding, D., Sanders, M., Lefebvre, P. A., Pei, J., Grishin, N. V., Vanderlaan, G., Billker, O. and Snell, W. J. 2013. Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates. Genes Dev. 27, 1198-1215. https://doi.org/10.1101/gad.212746.112
  107. Nishii, I., Ogihawa, S. and Kirk, D. L. 2003. A kinesin, InvA, plays an essential role in Volvox morphogenesis. Cell 113, 743-753. https://doi.org/10.1016/S0092-8674(03)00431-8
  108. Nishimura, Y. 2010. Uniparental inheritance of cpDNA and the genetic control of sexual differentiation in Chlamydomonas reinhardtii. J. Plant Res. 123, 149-162. https://doi.org/10.1007/s10265-009-0292-y
  109. Nishimura, Y., Higashiyama, T., Suzuki, L., Misumi, O. and Kuroiwa, T. 1998. The biparental transmission of the mitochondrial genome in Chlamydomonas reinhardtii visualized in living cells. Euro. J. Cell Biol. 77, 124-133. https://doi.org/10.1016/S0171-9335(98)80080-0
  110. Nishimura, Y., Misumi, O., Matsunaga, S., Higashiyama, T., Yokota, A. and Kuroiwa, T. 1999. The active digestion of uniparental chloroplast DNA in a single zygote of Chlamydomonas reinhardtii is revealed by using the optical tweezer. Proc. Natl. Acad. Sci. USA 26, 12577-12582.
  111. Nishimura, Y., Misumi, O., Kato, K., Inada, N., Higashiyama, T., Momoyama, Y. and Kuroiwa, T. 2002. An $mt^{+}$ gamete-specific nuclease that targets $mt^{-}$ chloroplasts during sexual reproduction in C. reinhardtii. Genes Dev. 16, 1116-1128. https://doi.org/10.1101/gad.979902
  112. Nishimura, Y., Shikanai, T., Nakamura, S., Kawai-Yamada. M. and Uchimiya, H. 2012. Gsp1 triggers the sexual developmental program including inheritance of chloroplast DNA and mitochondrial DNA in Chlamydomonas reinhardtii. Plant Cell 24, 2401-2414. https://doi.org/10.1105/tpc.112.097865
  113. Nozaki, H., Misawa, K., Kajita, T., Kato, M., Nohara, S. and Watanabe, M. M. 2000. Origin and evolution of the colonial Volvocales (Chlorophyceae) as inferred from multiple, chloroplast gene sequences. Mol. Phylogenet. Evol. 17, 256-268. https://doi.org/10.1006/mpev.2000.0831
  114. Onodera, A., Kong, S. G., Doi, M., Shimazaki, K. I., Christie J., Mochizuki, N. and Nagatani, A. 2005. Phototropin from Chlamydomonas reinhardtii is functional in Arabidopsis thaliana. Plant Cell Physiol. 46, 367-374. https://doi.org/10.1093/pcp/pci037
  115. Pan, J., Haring, M. A. and Beck, C. F. 1997. Characterization of blue light signal transduction chains that control development and maintenance of sexual competence in Chlamydomonas reinhardtii. Plant Physiol. 115, 1241-1249. https://doi.org/10.1104/pp.115.3.1241
  116. Pan, J., Misamore, M. J., Wang, Q. and Snell, W. J. 2003. Protein transport and signal transduction during fertilization in Chlamydomonas. Traffic 4, 452-459. https://doi.org/10.1034/j.1600-0854.2003.00105.x
  117. Pan, J. and Snell, W. J. 2000a. Regulated targeting of a protein kinase into an intact flagellum. An aurora/Ipl1p-like protein kinase translocates from the cell body into the flagella during gamete activation in Chlamydomonas. J. Biol. Chem. 275, 24106-24114. https://doi.org/10.1074/jbc.M002686200
  118. Pan, J. and Snell, W. J. 2000b. Signal transduction during fertilization in the unicellular green alga, Chlamydomonas. Curr. Opin. Microbiol. 3, 596-602. https://doi.org/10.1016/S1369-5274(00)00146-6
  119. Pasquale, S. M. and Goodenough, U. W. 1987. Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J. Cell Biol. 105, 2279-2292. https://doi.org/10.1083/jcb.105.5.2279
  120. Pazour, G. J., Dickert, B. L. and Witman, G. B. 1999. The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J. Cell Biol. 144, 473-481. https://doi.org/10.1083/jcb.144.3.473
  121. Pazour, G. J., Wilkerson, C. G. and Witman, G. B. 1998. A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT). J. Cell Biol. 141, 979-992. https://doi.org/10.1083/jcb.141.4.979
  122. Pijst, H. L. A., van Drie, R., Janssens, P. M. W., Musgrave, A. and van den Ende, H. 1984. Cyclic AMP is involved in sexual reproduction of Chlamydomonas eugametos. FEBS Lett. 174, 132-136. https://doi.org/10.1016/0014-5793(84)81091-1
  123. Porter, M. E., Bower, R., Knott, J. A., Byrd, P. and Dentler, W. 1999. Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol. Biol. Cell 10, 693-712. https://doi.org/10.1091/mbc.10.3.693
  124. Prochnik, S. E., Umen, J., Nedelcu, A. M., Hallmann, A. and Miller, S. M., et al. 2010. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329, 223-226. https://doi.org/10.1126/science.1188800
  125. Proschold, T., Harris, E. H. and Coleman, A. W. 2005. Portrait of a species: Chlamydomonas reinhardtii. Genetics 170, 1601-1610. https://doi.org/10.1534/genetics.105.044503
  126. Proschold, T., Marin, B., Schlosser, U. G. and Melkonian, M. 2001. Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta): I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152, 265-300. https://doi.org/10.1078/1434-4610-00068
  127. Qin, H., Burnette, D. T., Bae, Y. K., Forscher, P., Barr, M. M. and Rosenbaum, J. L. 2005. Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane. Curr. Biol. 15, 1695-1699. https://doi.org/10.1016/j.cub.2005.08.047
  128. Raven ,P. H., Evert, R. F. and Eichhorn, S. E. 2005. Biology of Plants, p. 330. 7th ed., WH Freeman and Company Pubishers, NJ, USA.
  129. Ryan, R., Grant, D., Chiang, K. S. and Swift, H. 1978. Isolation and characterization of mitochondrial DNA from Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 75, 3268-3272. https://doi.org/10.1073/pnas.75.7.3268
  130. Sager, R. 1954. Mendelian and non-mendelian inheritance of streptomycin resistance in Chlamydomonas reinhardi. Proc. Natl. Acad. Sci. USA 40, 356-363. https://doi.org/10.1073/pnas.40.5.356
  131. Sager, R. and Granick, S. 1954. Nutritional control of sexuality in Chlamydomonas reinhardi. J. Gen. Physiol. 54, 729-42.
  132. Sager, R. and Lane, D. 1972. Molecular basis of maternal inheritance. Proc. Natl. Acad. Sci. USA 69, 2410-2413. https://doi.org/10.1073/pnas.69.9.2410
  133. Saito, T., Small, L. and Goodenough, U. W. 1993. Activation of adenylyl cyclase in Chlamydomonas reinhardtii by adhesion and by heat. J. Cell Biol. 122, 137-147. https://doi.org/10.1083/jcb.122.1.137
  134. Serpe, M. D. and Nothnagel, E. A. 1999. Arabinogalactanproteins in the multiple domains of the plant cell surface. Adv. Bot. Res. 30, 207-289.
  135. Steele, R. E. and Dana, C. E. 2009. Evolutionary history of the HAP2/GCS1 gene and sexual reproduction in metazoans. PLoS One 4, e7680. https://doi.org/10.1371/journal.pone.0007680
  136. Tam, L. W., Wilson, N. F. and Lefebvre, P. A. 2007. A CDK-related kinase regulates the length and assembly of flagella in Chlamydomonas. J. Cell Biol. 176, 819-829. https://doi.org/10.1083/jcb.200610022
  137. Treier, U., Fuchs, S., Weber, M., Wakarchuk, W. W. and Beck, C. F. 1989. Gametic differentiation in Chlamydomonas reinhardtii: light dependence and gene expression patterns. Arch. Microbiol. 152, 572-577. https://doi.org/10.1007/BF00425489
  138. Uchida, H., Suzuki, L., Anai, T., Doi, K., Takano, H., Yamashita, H., Oka, T., Kawano, S., Tomizawa, K. I., Kawazu, T., Kuroiwa, H. and Kuroiwa, T. 1999. A pair of invertedly repeated genes in Chlamydomonas reinhardtii encodes a zygote-specific protein whose expression is UVsensitive. Curr. Genet. 36, 232-240. https://doi.org/10.1007/s002940050495
  139. Umen, J. G. 2011. Evolution of sex and mating loci: An expanded view from Volvocine algae. Curr. Opin. Microbiol. 14, 634-641. https://doi.org/10.1016/j.mib.2011.10.005
  140. Umen, J. G. 2014. Green algae and the origins of multicellularity in the plant kingdom. Cold Spring Harb. Perspect Biol. doi: 10.1101/cshperspect.a016170. pp 1-27.
  141. Walther, Z., Vashishtha, M. and Hall, J. L. 1994. The Chlamydomonas FLAIO gene encodes a novel Kinesin-homologous protein. J. Cell Biol. 126, 175-188. https://doi.org/10.1083/jcb.126.1.175
  142. Wang, Q. and Snell, W. J. 2003. Flagellar adhesion between mating type plus and mating type minus gametes activates a flagellar protein-tyrosine kinase during fertilization in Chlamydomonas. J. Biol. Chem. 278, 32936-32942. https://doi.org/10.1074/jbc.M303261200
  143. Wang, Q., Pan, J. and Snell, W. J. 2006. Intraflagellar transport particles participate directly in cilium-generated signaling in Chlamydomonas. Cell 125, 549-562. https://doi.org/10.1016/j.cell.2006.02.044
  144. Wegener, D. and Beck, C. F. 1991. Identification of novel genes specifically expressed in Chlamydomonas reinhardtii zygotes. Plant Mol. Biol. 16, 937-946. https://doi.org/10.1007/BF00016066
  145. Weiss, R. L., Goodenough, D. A. and Goodenough, U. W. 1977. Membrane differentiation at sites specialized for cell fusion. J. Cell Biol. 72, 144-160. https://doi.org/10.1083/jcb.72.1.144
  146. Wilson, N. F. and Snell, W. J. 1998. Microvilli and cell-cell fusion during fertilization.Trends Cell Biol. 8, 93-96. https://doi.org/10.1016/S0962-8924(98)01234-3
  147. Wilson, N. F., Foglesong, M. J. and Snell, W. J. 1997. The Chlamydomonas mating type plus fertilization tubule, a prototypic cell fusion organelle: isolation, characterization and in vitro adhesion to mating type minus gametes. J. Cell Biol. 137, 1537-1553. https://doi.org/10.1083/jcb.137.7.1537
  148. Wilson, N. F., O'Connell, J. S., Lu, M. and Snell, W. S. 1999. Flagellar adhesion between mt(+) and mt(-) Chlamydomonas gametes regulates phosphorylation of the mt(+)-specific homeodomain protein GSP1. J. Biol. Chem. 274, 34383-34388. https://doi.org/10.1074/jbc.274.48.34383
  149. Woessner, J. P. and Goodenough, U. W. 1989. Molecular characterization of a zygote wall protein: an extensin-like molecule in Chlamydomonas reinhardtii. Plant Cell 1, 901-911. https://doi.org/10.1105/tpc.1.9.901
  150. Wong, J. L. and Johnson, M. A. 2009. Is HAP2-GCS1 an ancestral gamete fusogen? Trends Cell Biol. 20, 134-141.
  151. Woodcock, C. L., Safer, J. P. and Stanchfield, J. E. 1976. Structural repeating units in chromatin. I. Evidence for their general occurrence. Exp. Cell Res. 97, 101-110. https://doi.org/10.1016/0014-4827(76)90659-5
  152. Wu, H., de Graaf, B., Mariani, C. and Cheung, A. Y. 2001. Hydroxyproline-rich glycoproteins in plant reproductive tissues: Structure, functions and regulation. Cell Mol. Life Sci. 58, 1418-1429. https://doi.org/10.1007/PL00000785
  153. van den Ende, H. and VanWinkle-Swift, K. P. 1994. Mating type differenentiation and mate selection in the homothallic Chlamydomonas monoica. Curr. Genet. 25, 209-216. https://doi.org/10.1007/BF00357164
  154. VanWinkle-Swift, K. P. and Rickoll, W. L. 1997. The zygospore wall of Chlamydomonas monoica (Chlorophyceae): morphogenesis and evidence for the presence of sporopollenin. J. Phycol. 33, 655-665. https://doi.org/10.1111/j.0022-3646.1997.00655.x
  155. von Besser, K., Frank, A. C., Johnson, M. A. and Preuss, D. 2006. Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133, 4761-4769. https://doi.org/10.1242/dev.02683
  156. Zhang, Y. and Snell, W. J. 1994. Flagellar adhesion-dependent regulation of Chlamydomonas adenylyl cyclase in vitro: a possible role for protein kinases in sexual signaling. J. Cell Biol. 125, 617-624. https://doi.org/10.1083/jcb.125.3.617
  157. Zhao, H., Lu, M., Singh, R. and Snell, W. J. 2001. Ectopic expression of a Chlamydomonas $mt^{+}$-specific homeodomain protein in $mt^{-}$ gametes initiates zygote development with out gamete fusion. Genes Dev. 15, 2767-2777. https://doi.org/10.1101/gad.919501